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NEUROFEEDBACK IN ADHD EDITED BY : Hartmut Heinrich, Ute Strehl, Martijn Arns, Aribert Rothenberger and Tomas Ros PUBLISHED IN : Frontiers in Human Neuroscience Frontiers Copyright Statement About Frontiers © Copyright 2007-2016 Frontiers Media SA. All rights reserved. Frontiers is more than just an open-access publisher of scholarly articles: it is a pioneering All content included on this site, approach to the world of academia, radically improving the way scholarly research such as text, graphics, logos, button icons, images, video/audio clips, is managed. The grand vision of Frontiers is a world where all people have an equal downloads, data compilations and opportunity to seek, share and generate knowledge. Frontiers provides immediate and software, is the property of or is licensed to Frontiers Media SA permanent online open access to all its publications, but this alone is not enough to (“Frontiers”) or its licensees and/or realize our grand goals. subcontractors. 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With their international copyright laws. unique mix of varied contributions from Original Research to Review Articles, Frontiers The above represents a summary only. For the full conditions see the Research Topics unify the most influential researchers, the latest key findings and historical Conditions for Authors and the Conditions for Website Use. advances in a hot research area! Find out more on how to host your own Frontiers ISSN 1664-8714 Research Topic or contribute to one as an author by contacting the Frontiers Editorial ISBN 978-2-88919-722-4 DOI 10.3389/978-2-88919-722-4 Office: [email protected] Frontiers in Human Neuroscience 1 January 2016 | Neurofeedback in ADHD NEUROFEEDBACK IN ADHD Topic Editors: Hartmut Heinrich, University of Erlangen-Nürnberg, Germany Ute Strehl, University of Tübingen, Germany Martijn Arns, Utrecht University, Netherlands Aribert Rothenberger, University Medical Center Göttingen, Germany Tomas Ros, University of Geneva, Switzerland Image by Martijn Arns EEG-based neurofeedback is used as a treatment approach in attention-deficit / hyperactivity disorder (ADHD), a clinically and pathophysiologically heterogeneous child psychiatric disorder. There is increasing evidence for specific effects of neurofeedback when applying ‘standard’ pro- tocols (slow cortical potentials, theta/beta, sensorimotor rhythm). Knowledge about underlying mechanisms and moderating variables is increasing. Nevertheless, further well-controlled and conducted trials are needed to answer open questions concerning optimisation and individu- alisation of neurofeedback. Further improvements may develop with new methods and tech- nical developments (e.g., tomographic neurofeedback) and new concepts (integrated ADHD treatment). Frontiers in Human Neuroscience 2 January 2016 | Neurofeedback in ADHD This Frontiers Research Topic comprising 14 articles intends to answer the following questions concerning neurofeedback in ADHD: • How efficacious is neurofeedback? • What is the rationale of applying a certain neurofeedback protocol in ADHD? • What are central mechanisms and which moderating variables may affect training and treat- ment outcome? • How to optimise treatment? What are new developments and which benefits may be expected? Aspects of learning theory are also stressed dissociating ‘neurofeedback as a treatment’ and ‘neurofeedback as entertainment’. In the Editorial, this crucial aspect is compared to the way you read (and study) a scientific book versus reading a thriller for leisure. In this respect: Enjoy this Research Topic, study and apply it in practice, unless you read it for entertainment purposes! Citation: Heinrich, H., Strehl, U., Arns, M., Rothenberger, A., Ros, T., eds. (2016). Neurofeedback in ADHD. Lausanne: Frontiers Media. doi: 10.3389/978-2-88919-722-4 Frontiers in Human Neuroscience 3 January 2016 | Neurofeedback in ADHD Table of Contents 06 Editorial: Neurofeedback in ADHD Martijn Arns, Hartmut Heinrich, Tomas Ros, Aribert Rothenberger and Ute Strehl Reviews, theoretical and opinion papers etc. 09 Pathophysiology of ADHD and associated problems—starting points for NF interventions? Björn Albrecht, Henrik Uebel-von Sandersleben, Holger Gevensleben and Aribert Rothenberger 23 Neurofeedback in attention-deficit/hyperactivity disorder – different models, different ways of application Holger Gevensleben, Gunther H. Moll, Aribert Rothenberger and Hartmut Heinrich 33 What learning theories can teach us in designing neurofeedback treatments Ute Strehl 41 Are treatment effects of neurofeedback training in children with ADHD related to the successful regulation of brain activity? A review on the learning of regulation of brain activity and a contribution to the discussion on specificity Agnieszka Zuberer, Daniel Brandeis and Renate Drechsler 56 Tuning pathological brain oscillations with neurofeedback: A systems neuroscience framework Tomas Ros, Bernard J. Baars, Ruth A. Lanius and Patrik Vuilleumier 78 What future research should bring to help resolving the debate about the efficacy of EEG-neurofeedback in children with ADHD Madelon A. Vollebregt, Martine van Dongen-Boomsma, Dorine Slaats-Willemse and Jan K. Buitelaar 84 EEG-based local brain activity feedback training—tomographic neurofeedback Herbert Bauer and Avni Pllana Methodical studies 90 EEG spectral analysis of attention in ADHD: Implications for neurofeedback training? Hartmut Heinrich, Katrin Busch, Petra Studer, Karlheinz Erbe, Gunther H. Moll and Oliver Kratz 100 Neurofeedback of slow cortical potentials: Neural mechanisms and feasibility of a placebo-controlled design in healthy adults Holger Gevensleben, Björn Albrecht, Henry Lütcke, Tibor Auer, Wan Ilma Dewiputri, Renate Schweizer, Gunther Moll, Hartmut Heinrich and Aribert Rothenberger Frontiers in Human Neuroscience 4 January 2016 | Neurofeedback in ADHD 113 Slow cortical potential and theta/beta neurofeedback training in adults: Effects on attentional processes and motor system excitability Petra Studer, Oliver Kratz, Holger Gevensleben, Aribert Rothenberger, Gunther H. Moll, Martin Hautzinger and Hartmut Heinrich Clinical studies 126 EEG neurofeedback treatments in children with ADHD: An updated meta- analysis of randomized controlled trials Jean-Arthur Micoulaud-Franchi, Pierre Alexis Geoffroy, Guillaume Fond, Régis Lopez, Stéphanie Bioulac and Pierre Philip 133 Differential effects of theta/beta and SMR neurofeedback in ADHD on sleep onset latency Martijn Arns, Ilse Feddema and J. Leon Kenemans 143 Slow cortical potential neurofeedback and self-management training in outpatient care for children with ADHD: Study protocol and first preliminary results of a randomized controlled trial Hanna Christiansen, Verena Reh, Martin H. Schmidt and Winfried Rief 158 Near-infrared spectroscopy (NIRS) neurofeedback as a treatment for children with attention deficit hyperactivity disorder (ADHD)—a pilot study Anna-Maria Marx, Ann-Christine Ehlis, Adrian Furdea, Martin Holtmann, Tobias Banaschewski, Daniel Brandeis, Aribert Rothenberger, Holger Gevensleben, Christine M. Freitag, Yvonne Fuchsenberger, Andreas J. Fallgatter and Ute Strehl Frontiers in Human Neuroscience 5 January 2016 | Neurofeedback in ADHD EDITORIAL published:30October2015 doi:10.3389/fnhum.2015.00602 Editorial: Neurofeedback in ADHD MartijnArns1,2*,HartmutHeinrich3,4,TomasRos5,AribertRothenberger6andUteStrehl7 1ResearchInstituteBrainclinics,Nijmegen,Netherlands,2DepartmentofExperimentalPsychology,UtrechtUniversity, Utrecht,Netherlands,3DepartmentofChildandAdolescentMentalHealth,UniversityHospitalofErlangen,Erlangen, Germany,4kbo-Heckscher-Klinikum,München,Germany,5LaboratoryforNeurologyandImagingofCognition,Department ofNeurosciences,UniversityofGeneva,Geneva,Switzerland,6ChildandAdolescentPsychiatry,UniversityMedicalCenter Göttingen,Göttingen,Germany,7InstituteofMedicalPsychologyandBehavioralNeurobiology,UniversityofTuebingen Tuebingen,Germany Keywords:neurofeedback,ADHD,operantconditioning,classicalconditioning,EEG Almost a century ago Ivan Pavlov laid the groundwork for what we now know as classical conditioning.Notlongafterthisfirstdescriptionofclassicalconditioning,andthefirstdescription of the human EEG by Berger (1929), early observations were made that the human EEG (alpha blockingresponse)couldbeclassicallyconditioned(DurupandFessard,1935;Loomisetal.,1936). This alpha blocking response consists of a desynchronization of the dominant alpha activity, presentduringaneyesclosed(ordark)condition,intoadesynchronizedlowvoltagebetaEEG(also seeRosetal.,2014,inthisresearchtopic).Moresystematicstudiesdemonstratedthatthealpha blockingresponsefulfilledallofthePavloviantypesofconditioning(JasperandShagass,1941a) andcouldnotbeexplainedbysensitization(KnottandHenry,1941).JasperandShagasstooktheir experimentsonestepfurther,showingthatusingtheseprinciplesofconditioning,subjectscouldbe taught“voluntarycontrol”overtheiralphablockingresponse,bypairingthelight-onsetnottoan auditorytone,buttoasub-vocalcommand(“block”;JasperandShagass,1941b).Intheirmostbasic form, these can be considered the first demonstrations of “neurofeedback” or voluntary control over the EEG based on basic learning principles. Some years after these initial studies, the first reportsemployingoperantlearningprinciplestoEEGwerereportedbyKamiya[voluntarycontrol ofalphapowerandalphapeakfrequency(Kamiya,1968)],McAdametal.[voluntarycontrolofthe contingentnegativevariation(CNV)orslowcorticalpotential(SCP)(McAdametal.,1966)],and Sterman (operant conditioning of the so-called sensori-motor rhythm (SMR) in cats, Wyrwicka andSterman,1968).Interestingly,fromahistoricalperspective,theseEEGparametersarestillthe focusofintensivestudyinneurofeedbackresearch,asthisresearchtopicnicelyillustrates. Neurofeedback as a therapeutic intervention has been most comprehensively investigated for the treatment of attention-deficit/hyperactivity disorder (ADHD), in line with the theme of this research topic. Leading from a review by Albrecht et al. (2015) on the neurophysiological Editedandreviewedby: background of this child psychiatric disorder, including its comorbidities, the efficacy of HaukeR.Heekeren, neurofeedback in the treatment of ADHD is discussed in great detail. The current controversy FreieUniversitätBerlin,Germany regarding the efficacy of neurofeedback in ADHD is centered on the fundamental question of *Correspondence: how it should be evaluated: namely, in accordance with the APA guidelines (used to evaluate MartijnArns psychologicaltreatments),oralongthelinesofdrugtreatments(requiringdouble-blindplacebo [email protected] controlleddesigns).Intheirperspectivearticle,Vollebregtetal.(2014)reviewthisissueinmore detail, alongside Gevensleben and colleagues who investigated the feasibility of a double-blind Received:03June2015 placebocontrolleddesignforSCPneurofeedback(Gevenslebenetal.,2014a).Afurtherinteresting Accepted:18October2015 approach was undertaken by Micoulaud-Franchi and colleagues, who report an updated meta- Published:30October2015 analysisofneurofeedbackstudiesinADHD(Micoulaud-Franchietal.,2014).Usingacomparable Citation: approachastheEuropeanADHDGuidelinesgroup(Sonuga-Barkeetal.,2013),theydemonstrated ArnsM,HeinrichH,RosT, significant small to medium effect sizes specifically for inattention, in line with an earlier meta- RothenbergerAandStrehlU(2015) analysisthatalsorevealedstrongesteffects for thesame domain(Arnsetal.,2009).Inaddition, Editorial:NeurofeedbackinADHD. Front.Hum.Neurosci.9:602. Christiansenandcolleaguesreportpreliminaryresultsofarandomizedcontrolledtrialcomparing doi:10.3389/fnhum.2015.00602 SCPneurofeedbacktoaself-managementprogram(Christiansenetal.,2014). FrontiersinHumanNeuroscience|www.frontiersin.org October2015|Volume9 Article602|6 Arnsetal. Editorial:NeurofeedbackinADHD As is clear from the historical studies mentioned above, andcolleaguesoriginallyreportprotocolspecificeffectsonmotor neurofeedback is built on the foundations of learning theory. systemexcitability,aswellasP3amplitudesandCNVamplitudes Therefore, it is crucial to dissociate “neurofeedback as a for Theta/Beta and SCP neurofeedback (Studer et al., 2014). treatment” from “neurofeedback as entertainment.” The Arnsandcolleaguesfurtherrevealthatalthoughclinicallyboth “neurofeedbackasentertainment”isanapproachpopularizedby SMR and Theta/Beta neurofeedback have similar effects, only manymoderndevicessuchastheMattelMindflex(keepaballin for SMR neurofeedback the clinical effects are mediated by theairusingyourbrainactivity)orconsumer-gradeEEGunits a normalization of sleep-onset latency, suggesting the clinical suchastheEmotivEpocwhichrunbrain-training“apps.”Inthe effectsofTheta/Betaneurofeedbackaremediatedviaadifferent same way as there is a difference between “reading a book” for mechanism(Arnsetal.,2014a). entertainment purposes and “studying a book” to learn how to Although the majority of current research has utilized apply a specific technique it is no different for neurofeedback. neurofeedback protocols that stem from before the twenty-first Unfortunately in some clinical studies the goal has been to century, it is also important to look ahead and acknowledge “entertain”childrenwith“EEG-drivengames,”ratherthanreally new developments. With respect to individualized treatment, it applying a learning procedure the children could benefit from may be adequate to adapt protocols as suggested by an EEG foralongerperiod.Inthisrespect,thecontributionsfromStrehl study of attention in Heinrich et al. (2014), and the theoretical (2014) and Zuberer et al. (2015) are important and valuable framework of Ros et al. (2014). Several contributions also contributions covering aspects of learning theory. Gevensleben introducenewandpromisingapproachestoneurofeedback,such and colleagues additionally discuss different neurocognitive as the contribution by Marx and colleagues, who compared modelsofhowneurofeedbackworks(Gevenslebenetal.,2014b). SCP neurofeedback with Near Infrared Spectroscopy (NIRS) Ros and colleagues go one step further by offering a firmly neurofeedback in children with ADHD, providing feedback neurophysiologicalaccount,proposinga“systemsneuroscience from a signal physiologically similar to the fMRI BOLD framework”fortuningpathologicalbrainoscillations(Rosetal., response (Marx et al., 2014). Also, the perspective article by 2014). Bauer and Pllana provides further insights and opportunities Up to now, most neurofeedback protocols in the treatment in the application of EEG-based tomographic neurofeedback, of ADHD (e.g., SMR, Theta/Beta, and SCP Feedback) have theoretically enabling feedback of more focal brain activity shown comparable effect sizes on ADHD domains such as (BauerandPllana,2014). inattention, impulsivity and hyperactivity (reviewed in Arns We hope that you will enjoy this research topic, study and et al., 2014b). In this research topic further indications for apply it in practice, unless you read it only for entertainment specificity of various neurofeedback protocols emerge. Studer purposes! REFERENCES andfeasibilityofaplacebo-controlleddesigninhealthyadults.Front.Hum. Neurosci.8:990.doi:10.3389/fnhum.2014.00990 Albrecht, B., Uebel-von Sandersleben, H., Gevensleben, H., and Rothenberger, Gevensleben, H., Moll, G. H., Rothenberger, A., and Heinrich, H. (2014b). A. (2015). Pathophysiology of ADHD, comorbid disorders and associated Neurofeedback in attention-deficit/hyperactivity disorder - different problems – starting points for Neurofeedback interventions? Front. Hum. models, different ways of application. Front. Hum. Neurosci. 8:846. doi: Neurosci.9:359.doi:10.3389/fnhum.2015.00359 10.3389/fnhum.2014.00846 Arns,M.,deRidder,S.,Strehl,U.,Breteler,M.,andCoenen,A.(2009).Efficacy Heinrich, H., Busch, K., Studer, P., Erbe, K., Moll, G. H., and Kratz, O. ofneurofeedbacktreatmentinADHD:theeffectsoninattention,impulsivity (2014). EEG spectral analysis of attention in ADHD: implications for and hyperactivity: a meta-analysis. Clin. EEG Neurosci. 40, 180–189. doi: neurofeedback training? Front. Hum. Neurosci. 8:611. doi: 10.3389/fnhum. 10.1177/155005940904000311 2014.00611 Arns, M., Feddema, I., and Kenemans, J. L. (2014a). Differential effects of Jasper,H.,andShagass,C.(1941a).Conditioningtheoccipitalalpharhythmin theta/betaandSMRneurofeedbackinADHDonsleeponsetlatency.Front. man.J.Exp.Psychol.28,373–387.doi:10.1037/h0056139 Hum.Neurosci.8:1019.doi:10.3389/fnhum.2014.01019 Jasper, H., and Shagass, C. (1941b). Conscious time judgments related to Arns, M., Heinrich, H., and Strehl, U. (2014b). Evaluation of neurofeedback conditionedtimeintervalsandvoluntarycontrolofthealpharhythm.J.Exp. in ADHD: the long and winding road. Biol. Psychol. 95, 108–115. doi: Psychol.28,503–508.doi:10.1037/h0059201 10.1016/j.biopsycho.2013.11.013 Kamiya,J.(1968).Consciouscontrolofbrainwaves.Psychol.Today1,56–60. Bauer, H., and Pllana, A. (2014). EEG-based local brain activity feedback Knott,J.R.,andHenry,C.E.(1941).TheConditioningoftheblockingofthealpha trainingâe”tomographic neurofeedback. Front. Hum. Neurosci. 12:8. doi: rhythmofthehumanElectroencephalogram28,134–144. 10.3389/fnhum.2014.01005 Loomis,A.L.,Harvey,E.N.,andHobart,G.(1936).Electricalpotentialsofthe Berger, H. (1929). Über das elektroenzephalogramm des menschen. Arch. humanbrain.J.Exp.Psychol.19,249. PsychiatryNervenkr.87,527–570.doi:10.1007/BF01797193 Marx,A.M.,Ehlis,A.C.,Furdea,A.,Holtmann,M.,Banaschewski,T.,Brandeis, Christiansen, H., Reh, V., Schmidt, M. H., and Rief, W. (2014). Slow cortical D., et al. (2014). Near-infrared spectroscopy (NIRS) neurofeedback as a potential neurofeedback and self-management training in outpatient care treatmentforchildrenwithattentiondeficithyperactivitydisorder(ADHD)-a for children with ADHD: Study protocol and first preliminary results pilotstudy.Front.Hum.Neurosci.8:1038.doi:10.3389/fnhum.2014.01038 of a randomized controlled trial. Front. Hum. Neurosci. 8:943. doi: McAdam, D. W., Irwin, D. A., Rebert, C. S., and Knott, J. R. (1966). 10.3389/fnhum.2014.00943 Conativecontrolofthecontingentnegativevariation.Electroencephalogr.Clin. Durup, G., and Fessard, A. I. (1935). L’électrencéphalogramme de l’homme. Neurophysiol.21,194–195. 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Neurosci. 8:894. doi: 10.3389/fnhum.2014. conductedintheabsenceofanycommercialorfinancialrelationshipsthatcould 00894 beconstruedasapotentialconflictofinterest. Studer,P.,Kratz,O.,Gevensleben,H.,Rothenberger,A.,Moll,G.H.,Hautzinger, M.,etal.(2014).Slowcorticalpotentialandtheta/betaneurofeedbacktraining Copyright©2015Arns,Heinrich,Ros,RothenbergerandStrehl.Thisisanopen- inadults:effectsonattentionalprocessesandmotorsystemexcitability.Front. access article distributed under the terms of the Creative Commons Attribution Hum.Neurosci.8:555.doi:10.3389/fnhum.2014.00555 License(CCBY).Theuse,distributionorreproductioninotherforumsispermitted, Vollebregt,M.A.,vanDongen-Boomsma,M.,Slaats-Willemse,D.,andBuitelaar, provided the original author(s) or licensor are credited and that the original J.K.(2014).Whatfutureresearchshouldbringtohelpresolvingthedebate publicationinthisjournaliscited,inaccordancewithacceptedacademicpractice. abouttheefficacyofeeg-neurofeedbackinchildrenwithADHD.Front.Hum. Nouse,distributionorreproductionispermittedwhichdoesnotcomplywiththese Neurosci.8:321.doi:10.3389/fnhum.2014.00321 terms. FrontiersinHumanNeuroscience|www.frontiersin.org October2015|Volume9|Article602|8 REVIEW published:24June2015 doi:10.3389/fnhum.2015.00359 Pathophysiology of ADHD and associated problems—starting points for NF interventions? BjörnAlbrecht*,HenrikUebel-vonSandersleben,HolgerGevensleben and AribertRothenberger DepartmentofChildandAdolescentPsychiatry,UniversityMedicalCenterGöttingen,Göttingen,Germany Attention deficit hyperactivity disorder (ADHD) is characterized by severe and age-inappropriate levels of hyperactivity, impulsivity and inattention. ADHD is a heterogeneous disorder, and the majority of patients show comorbid or associated problemsfromotherpsychiatricdisorders.Also,ADHDisassociatedwithcognitiveand motivational problems as well as resting-state abnormalities, associated with impaired brainactivityindistinctneuronalnetworks.Thisneedstobeconsideredinamultimodal treatment, of which neurofeedback (NF) may be a promising component. During NF, specificbrainactivityisfed-backusingvisualorauditorysignals,allowingtheparticipants to gain control over these otherwise unaware neuronal processes. NF may be used to directly improve underlying neuronal deficits, and/or to establish more general self- regulatory skills that may be used to compensate behavioral difficulties. The current Editedby: manuscript describes pathophysiological characteristics of ADHD, heterogeneity of MartijnArns, ADHD subtypes and gender differences, as well as frequently associated behavioral ResearchInstituteBrainclinics, Netherlands problems such as oppositional defiant/conduct or tic disorder. It is discussed how NF Reviewedby: maybehelpfulasatreatmentapproachwithinthesecontexts. RoumenKirov, InstituteofNeurobiology,Bulgarian Keywords:Neurofeedback(NF),ADHD,ODD/CD,ticdisorder,comorbidity,children,neurobiology AcademyofSciences,Bulgaria LeonKenemans, UtrechtUniversity,Netherlands Introduction *Correspondence: BjörnAlbrecht, DepartmentofChildandAdolescent DifficultieswithInattentionorHyperactivityandImpulsivityasthecoresymptomsofAttention Psychiatry,UniversityMedicalCenter deficit Hyperactivity disorder (ADHD) are a frequent psychosocial burden. With an early onset Göttingen,vonSieboldStraße5, duringchildhood,ADHDisoftenpersistingthroughoutlife.Itisaheterogeneousdisorder,anda 37075Göttingen,Germany challenge to treat. In light of this heterogeneity, the most promising treatment approach should [email protected] bemultimodalinnature(Tayloretal.,2004;Swansonetal.,2008).Pharmacologicalinterventions particularly with stimulants such as methylphenidate and amphetamine sulfate, as well as non- Received:06October2014 stimulants like Atomoxetine are highly effective in reducing ADHD symptoms (Banaschewski Accepted:02June2015 Published:24June2015 etal.,2006;Kingetal.,2006),butlong-termeffectivenessisstillquestionable(Molinaetal.,2009; van de Loo-Neus et al., 2011). In addition, side-effects, non-response and prejudice have raised Citation: AlbrechtB,Uebel-vonSandersleben interestinnon-pharmacologicaltreatmentoptions(Sonuga-Barkeetal.,2013;Daleyetal.,2014). H,GevenslebenHandRothenberger Neurofeedback (NF) as a non-pharmacological intervention for ADHD utilizes cognitive- A(2015)PathophysiologyofADHD behavioral therapeutic elements to gain access on and practice brain activity (Arns et al., andassociatedproblems—starting 2014). In an operant learning paradigm, specific neural activity is quantified by means of pointsforNFinterventions? Electro-Encephalography (EEG) or functional Magnetic Resonance Imaging (fMRI) and fed Front.Hum.Neurosci.9:359. doi:10.3389/fnhum.2015.00359 back in real time with an easily accessible optical or acoustic signal. In general, the participants FrontiersinHumanNeuroscience|www.frontiersin.org June2015|Volume9|Article359| 9

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Frontiers in Human Neuroscience | www.frontiersin.org. October 2015 | Volume 9 Using a comparable approach as the European ADHD Guidelines group (Sonuga-Barke et al., 2013), they demonstrated Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition,. DSM-5. Arlington, VA:
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